The Mechanism of PGPR on the Photosynthesis System, Plant Resistance and Biofertilizers

It is worth noting that there is a relationship between root bacteria stimulating plant growth and the plant’s tolerance to the presence of heavy elements in the soil. This may be indicated by what was stated in research that a lineage belonging to the genus Brevibacillus isolated from lead contaminated soil stimulate the growth of Trifolium pratense L by increasing the acid concentration Indole Acetic Acid (IAA), nitrogen and phosphorous accumulation and formation root nodes and fungal roots, above which reduce absorption lead [67]. In a later study, [68] on the interaction of Brevibacillus brevis root bacteria and a fungus Glomus mosseae isolated from contaminated soil with cadmium, the results indicated that besides stimulating plant growth, fungal roots formation (Arbuscular mycorrhizae AM) and their properties are activated. The researchers attributed the increased plant resistance to cadmium to an increase in the availability of elements such as phosphorous and potassium and a decrease in the concentration of many other elements including cadmium, chromium, manganese, copper, molybdenum, iron and nickel in plant tissues. When examining strains of PSB7, PSB1 and PSB10 of bacteria Bacillus isolated from alluvial soil laboratory demonstrated its ability to reducing chromium, dissolving phosphorous, zinc and iron, and stimulating growth the plant made researchers anticipate its contribution to stimulating growth plant in vine-contaminated soil, meaning it may improve plant resistance toxicity to the element [69]. The effect of inoculation was also evaluated basalts of Cr⁶⁺ Hexa resist bacteria after isolation from the root zone in soil contaminated with vines namely Pseudomonas sp. PsA4 and Bacillus sp. Ba32 to the Indian cabbage Brassica juncea. The results indicate that these strains stimulate plant growth, the growth different concentrations of chromium in the soil had the highest activation when inoculation with Pseudomonas sp. PsA4 but the two strains did not change the amount of chromium accumulated in the root total. The researchers concluded that these bacteria protect plants from the inhibitory effect of chromium [70]. One of the beneficial contributions to soil composition is that plant root cells secrete mucus materials to facilitate their passage in the soil and mucous materials contain six, five sugars and uronic acid, likewise the microorganism cells at the root level secrete additional mucus material and all of them form a gel that binds soil microorganisms and root microorganisms with root, this combination is sometimes known as “rhizosheath”. This composition is important, as the amount of water absorbed by the plant decreases continuously the water begins to contract the gel material, maintaining the stability of the hydraulic conductivity and at the same time the bonding of the root and microorganisms to it. This ensures that the soil composition is not exposed to erosion and is likely to prevent pathogens and other neighborhoods from reaching the soil root cells [71].

Volatile Organic Compounds (VOCs), characterized by low molecular weight and high vapor pressure, are produced by all organisms as part of normal metabolism, and play important roles in communication within and between organisms. Similar to the Azospirillum system, other systems using NPs have been studied, but to a lesser extent, such as Bacillus subtilis GB03 and B. amyloliquefaciens IN937a, where the results of one study on the promising herb Arabidopsis indicate that these two strains may stimulate plant growth by forming a mixture of volatile substances especially the 2,3-butanediol precursor complex and acetoin initiator, these in turn affect plant metabolism [72]. In a study examined the effects of VOCs released by three species of plant growth-promoting rhizobacteria (Pseudomonas fluorescens, Bacillus subtilis, Azospirillum brasilense) on growth parameters and composition of Essential Oils (EO) in the aromatic plant Mentha piperita [73]. The bacteria and plants were grown on the same Petri dish, but were separated by a physical barrier such that the plants were exposed only to VOCs but not to solutes from the bacteria. Growth parameters of plants exposed to VOCs of P. fluorescens or B. subtilis were significantly higher than those of controls or A. brasilense-treated plants. Production of EOs (monoterpenes) was increased 2-fold in P. fluorescens-treated plants. Two major EOs, (+)pulegone and (−)menthone, showed increased biosynthesis in P. fluorescens-treated plants. Menthol in A. brasilense-treated plants was the only major EO that showed a significant decrease. These findings suggest that VOCs of rhizobacteria, besides inducing biosynthesis of secondary metabolites, affect pathway flux or specific steps of monoterpene metabolism. Bacterial VOCs are a rich source for new natural compounds that may increase crop productivity and EO yield of this economically important plant species [74].

Plants inoculated with root stimulating bacteria appear fresh, vibrant, and greener than non-inoculated plants, indicating that the photosynthesis system is affected. Some research indicates for example, the inoculation of cabbage Brassica oleracea var. botrytis with biological fertilizers leads to an increase in the total chlorophyll content [75]. Likewise, wheat plants inoculated with Azospirillum and Bacillus increases the total chlorophyll content in the field [76]. The rice plant inoculated with Azospirillum brasilense NO40 isolated from Egyptian soil and the plant grown in China increases its chlorophyll content [77]. In the most comprehensive study of chlorophyll and other phytopigments [78] on wheat seedlings inoculated with A. brasilense Cd. The results showed that there was a significant increase in chlorophyll a, b and the pigments including, β-carotene, violaxanthin, zeaxanthin, antheroxanthin, lutein, and neoxanthin, in the first week after inoculation, either with liquid inoculation or in the form of alginate microbeads.

As for “control”, a general review sums up [79] that under another group of root bacteria stimulating plant growth, the plant is activated in an indirect way, preventing the harmful effect of microorganisms and pathogens on the plant. Other review [29] indicated it is the bacteria in this group that stimulate plant growth indirectly through the formation of compounds harmful to other organisms (bacteria, fungi and viruses) which are not harmful to plants, or limit the availability of some essential elements for these harmful organisms, or plant inductions to increase plant resistance to disease..

Traditionally, methyl bromide is used to sterilize soil to eliminate plant pathogens when planting it, as a result of the devastating effect of this compound on the ozone layer after its volatilization, many people and environmental preservation agencies were interested in that. They demanded to stop its use, and some governments responded and enacted laws limiting its use so that it gradually stopped using, so in the United States of America, the use of this compound was stopped since 2001 [80]. Further claim by reducing the use of chemicals and fertilizers in traditional agricultural practices. The trend was towards finding alternatives to the use of this compound that were not harmful to the environment. So, the best candidate to control this was the group of “root bacteria stimulating plant growth”, a candidate to play the role of sterilizing and reducing material use chemical and fertilizers, from which this group is still a wide field of scientific research. Hence, research in the field of control was so prevalent in the eighties of the twentieth century AD, a tremendous momentum of research and reviews emerged about the ability of “root bacteria stimulant for plant growth” to reduce the number of harmful microorganisms in the rhizospher and thus produce stimulation of plant growth [31] This research in this field resulted in the introduction of a new term, which is “harmful root bacteria”, meaning “Deleterious Rhizobacteria” (DRB), to assume that there are bacteria in the root zone causing damage to the plant (inhibiting its normal growth). Then accordingly, inoculating the plant with “root bacteria stimulating plant growth” will inhibits these bacteria and thus stimulates plant growth.

Such an assumption is not correct until now, as it means that there are strains of “harmful root bacteria” that can be isolated and proven harmful according to the rules of infection the pathogen that is based on the definition of the pathogen as defined by the scientist Koch’s definition. A description of the group has not yet been published symptoms of damage associated with the use of the so-called “harmful root bacteria”, moreover, most of this research was not under competitive environmental conditions or that the inoculation used contains huge numbers of organisms (about the logarithm of 8.7 bacteria to 11.8 bacteria in inoculation medium), this of course does not represent natural soil competition [31] Scientists are beginning to realize the basic mistakes in research on “harmful root bacteria” and this is still the field that is researched, but to a lesser extent, as the number of studies gradually decreased in the 1990s from the twentieth century AD.

Of the microorganisms present in the soil and which propagate it producer of antibiotics [81] Pseudomonas, Streptomyces, Sorangium, Arthrobacter, Nocardia, Burkholderia, Brevibacterium and others. It is the most well-known microorganism characterized by the formation of antagonists the pathogenic of the genus Pseudomonas.sp, which is also considered as organisms associated with plant roots, and can refer to the previous source, which covers primary studies and lists of organisms that have been observed to be antibiotics [81]. One of the first studies that demonstrates direct antagonism and induction of plant resistance to the pathogen and the formation of an antibiotic was shown by a study on root bacteria stimulating plant growth Pseudomonas fluorescens with an antibiotic composition is phenazine, which is against the pathogenic fungus Gaeumannomyces graminis var. tritici, which causes Take-all stem disease of wheat plants [82]. Then research continued to clear the root rhizobacteria in search of bacteria that stimulates growth and has an anti-organism effect the pathogen of the plant. Modern techniques such as the use of microscopy immunofluorescence and reporter genes have contributed in improving field studies of inoculation with the bacterium of the genus Pseudomonas and broadening knowledge about its behavior in this environment [83]. It is noted that surveying a large number of members of the bacterial community around the roots of a plant may lead to obtaining isolates with high capacities that contribute to the benefit of the plant in all stages of its growth and exposure to disease. This is reported by a survey in the survey vegetable chili peppers and tomato susceptible to peptic degeneration disease before and after treatment with a fungus of the genus Pythium sp. and Phytophthora sp. Strains of the bacterium were selected Pseudomonas sp, which is FQP PB-3, FQA PB-3, and GRP (3). It was reported that these strains stimulated growth and reduced the incidence rate to a large extent for both plants [84]. Added to this is a study on lettuce that is exposed to infection by the fungus Fusarium?. sp. 12 isolates of ?Pseudomonas sp. were found has anti-fungal activity, but only three of them activated growth in the plant [83].

Some previous studies reported that cyanide formation is a major and direct agent in antagonism against the Pseudomonas fluorescens, Rhizotrophin strains CHAO, that was also associated with the pathogen of the tobacco plant Thielaviopsis basicola black root rot occurs without the plant being affected [84] and induces the formation of cyanide by increasing the concentration triple iron [85]. A Systemic Acquired Resistance (SAR) develops in the plant after initial infection with a pathogen, i.e., uninfected areas of the plant body those who have been infected will gain greater resistance to the pathogen again and salicylic acid contributes to its pathway [86]. On the other hand, some research has reported that strains of root growth stimulating bacteria induces systemic resistance in the shoot system when the roots are infected with a pathogen, as this has been observed in many types of plants such as beans, cloves, cucumbers and others [87]. Characterized this type of resistance as the rhizobacteria-mediated Induced Systemic Resistance (ISR). A review indicates that this mode of resistance, particularly in the herbivore Arabidopsis thaliana has both jasmonic acid and ethylene play an effective role in the pathway of the excitation signal from the roots to the shoots [86].

After mentioning some researches and their results after inoculation, there are many opinions and proposals to explain the phenomenon of activation as discussed in some reviews [88,89], they include:
A. Increase in nitrogen fixation.
B. Production of growth regulators; auxin, gibberellin, cytokinin and ethylene.
C. Dissolving phosphorus and sulfur oxidation.
D. Increase the availability of nitrates.
E. Production of extracellular antibiotics.
F. Production of hydrolyzed enzymes.
G. Hydrocyanide acid production.
H. Increase root permeability.
I. Tight competition for available nutrients at a site root.
J. Induction of systemic plant resistance.

Another possibility adds another mechanism: change the composition of the bacterial community around the root as a result of pollinator addition. This research reported [90] that when two soil types were used for European alder and inoculation with Bacillus licheniformis the response was different, as in one type of soil the leaf area increased significantly, while the other growth parameters (root growth, for example), the response did not differ, in addition to the disappearance of the inoculation bacterium in the first soil after 6 weeks, while on the other soil after only two weeks. From here it was concluded that the revitalization of growth was a change the bacterial community in or around the root, however, before doing so it is important to consider the composition of the soil and the availability of the necessary elements for the plant. Which may support the role of changing the bacterial community around the roots, other research reported on Quercus ilex ssp. ballota oak seedlings and co-inoculation with rhizobacteria strains plant growth stimulant Bacillus licheniformis CECT 5106 and the fungus Pisolithus tinctorius, which is usually symbiotic with these trees, that although growth was stimulated, the growth of the fungus was inhibited and changed slightly both the total bacterial community around the roots and the potential cultivated bacterial individuals [91].

Despite the abundance of research on this topic on the various physiological and molecular phenomena of these strains root bacteria stimulating plant growth all proposals and opinions to explain this phenomenon, but the general picture is its ability to fix nitrogen when cultivated and when it is associated with the plant, [31]. Before that, some scientists [92] believed that the mechanism of reducing the severity of the disease by root bacteria stimulated the growth of the plant as an effective biological control agent may be the result of a combination of several mechanisms but not standardized with a specific name. After that, I directly put forward the hypothesis that there are several mechanisms that affect each one of them are few, and these mechanisms cooperate with some in influencing addition, and it can be called the “synergy” hypothesis or the ”Additive theory”. In the Encyclopedia of Soils in the Environment [29] several mechanisms were mentioned (about 16 mechanisms) each one could be a mechanism that explains the observation of one to affect after inoculation with one or a mixture of bacteria of the roots or the rhizobacteria or internal bacteria such as nitrogen fixation or the production of growth regulators and others. At the moment there is no general agreement on a specific mechanism, although the production of the growth regulator of Indole Acetic Acid (IAA) may explain what has been observed in the increase in root length, the number of root hairs, root branches and the surface area of the roots of the treated seedlings, but other growth regulators such as gibberellin and nitrogen fixation may also increase productivity and contribute to the availability and uptake of some nutrients by the treated plant [31].

Several autotrophic bacteria have been described and studied nitrogenous and non-symbiotic and tested for use as a bio-fertilizer such as BioGro as mentioned in a previous review [43], for more on this, see also [44]. Likewise, the results and indications of these researches about the groups of bacteria associated with the plant and stimulate its growth were exploited, so that a number of commercial inoculations were available on the market to stimulate the growth of a specific plant (corn, wheat and rice) or a group of crop plants and tree nurseries, Table 2 represents such inoculations, for example, are not limited to. Although there are studies on the use of strains of the genus Pseudomonas in understanding general aspects of the influence mechanism, its use limits its lifetime (within several weeks) [93]. Some field studies indicate after inoculation with the bacterium Azospirillum suggests that 30 to 40% of inoculation operations are unsuccessful and that the increase in yield ranges from 5 to 30% only [29], although this genus is not specific to a specific plant but is rather broad and stimulates the growth of many plants as mentioned in this review. Also, a commercial product has been marketed in Sweden, Cedomon BioAgri AB, Uppsala (Sweden) to provide protection from pathogens carried by barley and oats seeds by treating the seeds with strain inoculation Pseudomonas chlororaphis, which produces the antibiotic phenazine [94].

Table 2:Some examples of commercially available inoculations and effective bacteria [93].

In general, field applications of plant growth stimulating bacteria produce satisfactory benefits only under controlled conditions, but not under conditions and agricultural practices. Hence, it is important to optimize the selection and quality of the inoculation when a specific application is required, because the effectiveness of selection of nitrogen-fixing and stimulating rhizobacteria is crucial to the development of this technique [23]. An example of this is reported by a study on late leaf spot disease of the peanut plant Arachis hypogaea, which uses the fungicide chlorothalonil for its resistance in the field. This study reported that the combination of inoculation with a vaccine containing a strain of the root bacterium Pseudomonas aeruginosa GSE18 and tolerance to the fungicide and a quarter of the fungicide concentration (2000 micrograms/liter) and in a field treatment that doubled the productivity [95].

Bacteria with multiple benefits can be advantageous in commercial agriculture and are relevant to the bio-economy. Many cultivated plants of economic significance are grown in monoculture and require amendments for optimal growth and highly yield, as well as protection against disease organisms [96,97].

Increasing yield and decreasing fertilizer inputs

Utilization of bacterial consortia has inconsistent effects on crop yield [98]. It is known that the mixing of a bacterium (B. amyloliquefaciens) with a fungus (Trichoderma virens) improves yields of corn and tomato, among other crops [99,100] and is available in the market place. The company Excalibre-SA (ABM) combines Trichoderma with Bradyrhizobium for improved growth of soybean while BioGrow Endo (Mycorrhizal Applications) combines arbuscular mycorrhizal fungi and Trichoderma for improved growth and treatment of pathogens microorganisms involved in the soil; both of which are commercially available. A consortium of bacteria (Bacillus cereus PX35, Bacillus subtilis SM21, and Serratia sp XY2) reduced the incidence of root knot nematode (Meloidogyne incognita) in tomato, increased fruit yield (31.5 to 39%) and quality (soluble sugars, vitamin C, and titratable acids) [101]. Inoculation with N-fixing bacteria (Azospirillum and Azobacter) allowed halfrate N-fertilizer application and increased sesame seed yield and oil quality [102]. Similar effects were shown for the bacterium Azospirillum vinelandii inoculated Brassica carinata cv. Peela raya [103,104]. On the other hand, biofuels are derived from non-food biomass [105], often lignocellulosic material, to minimize any competition with food production; the long-term goal is provision of renewable fuels, along with high value bio-products, to reduce the atmospheric CO₂ emissions associated with fossil fuels [106]. With the use of PGPR that contain natural potential to cope with soil contaminants, the biofuel crops could be used efficiently for phytoremediation and also to reduce high levels of agrochemicals residues in agriculture lands [107]. Conversion of lignocellulosic material to fuel needs to become easier and less expensive to make this biologically fuel economically competitive [108]; in addition to that, there needs to be improved biomass availability from purposegrown biomass crops (e.g., Miscanthus, switchgrass, and Sorghum bicolour) [109,110]. The growth and productivity of selected grown biofuel crops can be improved through inoculation with PGPR [11] as has been demonstrated for switchgrass [111-114]. Marginal and contaminated lands can be used to grow biofuel crops in order to avoid conflicts around the food versus energy crops.

Plant disease control and rationalize agrochemicals consumption

One of the tangible benefit of PGPR is the Improving Disease Control and Reducing the Use of Agrochemicals. Biologicals are an alternative method for combating plant pathogens [115], and there are commercially available examples [116]. Beneficial rhizobacteria may secrete antibiotics and other compounds antagonistic to plant pathogens. Production of antibiotics is one of the more common biocontrol mechanisms [117,118]. There are commercially available examples of biocontrol agents [116]. However, microbes pathogens often develop resistance to the antibiotics and other mechanisms of biocontrol, so that they cannot be fully controlled in the long-term. A holistic approach with multiple controlling methods is probably better than excessive dependency on a single solution when confronting pathogens. Over the long term, pathogen-antagonistic bacteria will also evolve their mode of action to counteract the pathogens. PGPR also produce antibiotics such as lipopeptides, polyketides and antifungal metabolites that suppress pathogens [119].

1. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, et al. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409): 86-90.
2. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14(6): 209.
3. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4): 790-803.
4. Lebeis SL (2014) The potential for give and take in plant-microbiome relationships. Front Plant Sci 5: 287.
5. Bulgarelli D, Garrido-Oter R, Munch PC, Weiman A, Droge J, et al. (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3): 392-403.
6. Smith DL, Subramanian S, Lamont JR, Bywater-Ekegard M (2015) Signaling in the phytomicrobiome: Breadth and potential. Front Plant Sci 6: 709.
7. Smith DL, Gravel V, Yergeau E (2017) Editorial: Signaling in the phytomicrobiome. Front Plant Sci 8: 611.
8. Berg G, Rybakova D, Grube M, Koberl M (2016) The plant microbiome explored: Implications for experimental botany. J Exp Bot 67(4): 995-1002.
9. Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, et al. (2016) Getting the hologenome concept right: An eco-evolutionary framework for hosts and their microbiomes. mSystems 1(2): e00028-e00016.
10. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: Looking back and future perspectives. Front Microbiol 5: 148.
11. Smith DL, Praslickova D, Ilangumaran G (2015) Inter-organismal signaling and management of the phytomicrobiome. Front. Plant Sci 6: 722.
12. Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, et al. (2018) Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9: 1473.
13. Huisman OC (1982) Interrelations of root growth dynamics to epidemiology of root-invading fungi. Annual Review of Phytopathology 20: 303-327.
14. Lynch JM, Whipps JM (1991) Substrate flow in the rhizosphere. In: Keister DL, Cregan B (Eds.), The Rhizosphere and Plant Growth(Beltsville Symposia in Agricultural Research, BSAR Volume 14), Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 15-24.
15. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84: 827-837.
16. Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J. Exper. Botany 56(417): 1729-1739.
17. Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology and Biochemistry 33(11): 1437-1445.
18. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, et al. (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: Plant-dependent enrichment and seasonal shifts revealed. Applied and Environmental Microbiology 67(10): 4742-4751.
19. Yang CH, Crowley DE (2000) Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Applied and Environmental Microbiology 66(1): 345-351.
20. Yang CH, Crowley DE, Menge JA (2001) 16S rDNA fingerprinting of rhizosphere bacterial communities associated with healthy and Phytophthora infected avocado roots. FEMS Microbiology Ecology 35(2): 129-136.
21. Passioura JB (2006) Rhizosphere biology and crop productivity. Australian Journal of Soil Research 44(4): 299-317.
22. Cook RJ (2002) Advances in plant health management in the twentieth century. Ann Rev Phytopathol 38: 95-116.
23. Barea JM, Pozo MJ, Azcon R, Anguilar CA (2005) Microbial co-operation in the rhizosphere. J Exp Botany 56(417): 1761-1778.
24. Germida JJ, Siciliano SD, de Freitas JR, Seib AM (1998) Diversity of root-associated bacteria associated with field-grown canola (Brassica napus ) and wheat (Triticum aestivum). FEMS Microbiol Ecol 26(1): 43-50.
25. Rondon MR, Goodman RM, Handelsman J (1999) The earth’s bounty: Assessing and accessing soil microbial diversity. Trends Biotechnol 17(10): 403-409.
26. Manefield M, Whiteley AS, Griffiths RI, Bailey MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Applied and Environmental Microbioloy 68(11): 5367-5373.
27. Lueders T, Manefield M, Friedrich MW (2004) Enhanced sensitivity of DNA-and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environmental Microbiology 6(1): 73-78.
28. Bloemberg GV, Lugtenberg, BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4(4): 343-350.
29. Bashan Y, de-Bashan LE (2005) Bacteria/plant growth promotion. Encyclopedia of Soils in the Environment, Elsevier, Oxford, UK, pp. 103-115.
30. Kishore GK, Pande S, Podile AR (2005) Phylloplane bacteria increase seedling emergence, growth and yield of field-grown groundnut (Arachis hypogaea L). Letters in Applied Microbiology 40(4): 260-268.
31. Kloepper JW (2003) A Review of mechanisms for plant growth promotion by PGPR. 6^th International PGPR Workshop, Calicut, India, pp. 81-92.
32. Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. Proceedings of the 4^th International Conference on Plant Pathogenic Bacteria, Angers, France, pp. 879-882.
33. Bashan Y, Holguin G (1997) Azospirillum-plant relationships environmental and physiological advances (1990-1996). Can. J Microbiol 43(2): 103-121.
34. Vande Broek A, Dobbelaere S, Vanderleyden J, Van Dommelen A (2000) Azospirillum-plant root interactions signaling and metabolic interactions. In: Triplett EW (Ed.), Prokaryotic Nitrogen Fixation: A Model System for the Analysis of a Biological Process. Horizon Scientific Press, Wymondham, UK, pp.761-777.
35. Holguin G, Patten CL, Glick BR (1999) Genetics and molecular biology of Azospirillum. Biol Fertil Soils 29: 10-23.
36. James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res 65(2-3): 197-209.
37. Dobbelaere S, Croonenborghs A, Thys A, Ptacek A Vanderleyden J, et al. (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28(9): 871-879.
38. Kennedy IR, Islam N (2001) The current and potential contribution of asymbiotic nitrogen fixation to nitrogen requirements on farms: A review. Aust J Exp Agric 41(3): 447-457.
39. Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Canadian Journal of Microbiology 50(8): 521-577.
40. Botelho GR, Mendonça-Hagler LC (2006) Fluorescent Pseudomonads associated with the rhizosphere of crops -An Overview. Brazilian Journal of Microbiology 37: 401-416.
41. Fallik E, Sarig S, Okon Y (1994) Morphology and physiology of plant roots associated with Azospirillum. In: Okon Y (Ed.), Azospirillum/Plant Associations, CRC Prees, Boca Raton, Florida, USA, pp. 77-85.
42. Bashan Y (2000) Environmental application for Azospirillum Proceedings of the 5^th International plant growth promoting rhizobacteria conference.
43. Al-Whaibi MH (2005) Plants and diazotrophic bacteria. King Saud University Journal (Agriculture Section) 5(2): 60-73.
44. Kennedy IR, Choudhury ATM, Kecskes ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: Can their potential for plant growth promotion be better exploited? Soil Biology & Biochemistry 36(8): 1229-1244.
45. Seshadri S, Muthukumarasamy R, Lakshminarasimhan C, Ignacimuthu S (2000) Solubilization of inorganic phosphates by Azospirillum halopraeferans. Curr Sci 79(5): 565-567.
46. Tripura C, Sashidhar B, Podile AR (2007) Ethyl methanesulfonate mutagenesis-enhanced mineral phosphate solubilization by groundnut-associated Serratia marcescens GPS-5. Curr Microbiol 54(2): 84-79.
47. Hernandez ME, Kappler A, Newman DK (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70(2): 921-928.
48. Lin W, Okon Y, Ralph W, Hardy F (1983) Enhanced mineral uptake by Zea mays and Sorghum bicolor roots Inoculated with Azospirillum brasilense. Applied and Environmental Microbiology 45(6): 1775-1779.
49. Barton LL, GV Johnson, SO Miller (1986) The effect of Azospirillum brasilense on iron absorption and translocation by sorghum. J Plant Nutr 9(3-7): 557-565.
50. Bashan Y, Harrison SK, Whitmoyer RE (1990) Enhanced growth of wheat and soybean plants inoculated with Azospirillum brasilense is not necessarily due to general enhancement of mineral uptake. Applied and Environmental Microbiology 56(3): 769-775.
51. Bashan Y, Levanony H (1991) Alterations in membrane potential and in proton efflux in plant roots induced by Azospirillum brasilense. Plant and Soil 137: 99-103.
52. Puente ME, Li CY, Bashan Y (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants, II. Growth promotion of cactus seedlings. Plant Biology 6(5): 643-650.
53. Puente ME, Bashan Y, Li CY, Lebsky VK (2004) Microbial populations and activities in the rhizoplane of rock weathering desert plants, I. Root colonization and weathering of igneous rocks. Plant Biology 6: 629-642.
54. Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant and Soil 287: 15-21.
55. Arshad M, Frankenberger WT (1998) Plant growth promoting substances in the rhizosphere: Microbial production and function. Advances in Agronomy 62: 45-151.
56. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentration by plant growth promoting bacteria. J Theor Biol 190(1): 63-68.
57. Hall JA, Peirson D, Ghosh S, Glick BR (1996) Root elongation in various agronomic crops by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Israel Journal of Plant Sciences 49(1): 37-42.
58. Pallai R (2005) Effect of plant growth-promoting-rhizobacteria on canola (Brassica napus. L) and lentel (Lens culinaris. Medik) plants. Master of Science, Department of Applied, Microbiology and Food Science, University of Saskatchewan, Saskatoon, Saskatchewan.
59. Aslantas R ,Cakmakci R, Sahin F (2007) Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Scientia Horticulturae 111(4): 371-377.
60. Freitas SS, Aguilar Vildoso CI (2004) Rhizobacteria and growth promotion of citrus plants. Rev Bras Ciênc Solo 28(6): 987-994.
61. Khalid A, Arshad M, Zahir, ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. Journal of Applied Microbiology 96(3): 473-480.
62. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Letters in Applied. Microbiology 42(2): 155-159.
63. Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43(5): 1774-1781.
64. Lucas Garcia JA, Probanza A, Ramos B, Barriuso J, Gutierrez Mañero FJ (2004) Effects of inoculation with Plant Growth Promoting Rhizobacteria (PGPRs) and Sinorhizobium fredii on biological nitrogen fixation, nodulation and growth of Glycine max Osumi. Plant and Soil 267: 143-153.
65. Marulanda A, Barea J, Azcon R (2006) An indigenous drought-tolerant strain of glomus intraradices associated with a native bacterium improves water transport and root development in retama sphaerocarpa. Microbial Ecology 52(4): 670-678.
66. Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66(8): 3393-3398.
67. Vivas A, Azcon R, Biro B, Barea JM, Ruiz-Lozano JM (2003) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense under lead toxicity. Can. J Microbiol 49(10): 577-588.
68. Vivas A, Barea JM, Azcon R (2005) Interactive effect of Brevibacillus brevis and Glomus mosseae, both isolated from Cd contaminated soil, on plant growth, physiological mycorrhizal fungal characteristics and soil enzymatic activities in Cd polluted soil. Environmental Pollution 134(2): 257-266.
69. Wani PA, Khan MS, Zaidi A (2007) Chromium reduction plant growth-promoting potentials, and metal solubilizatrion by Bacillus sp. isolated from alluvial soil. Current Microbiology 54(3): 237-243.
70. Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr⁶⁺ on the growth of Indian mustard. Chemosphere 62(5): 741-748.
71. Czarnes S, Hallett PD, Bengough AG, Young IM (2000) Root- and microbial-derived mucilages affect soil structure and water transport. European Journal of Soil Science 51(3): 435-443.
72. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei H-X, et al. (2003) Bacterial volatiles promote growth in Arabidopsis. PNAS 100(8): 4927-4932.
73. Santoro M, Zygadlo J, Giordano W, Banchio E (2011) Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiology and Biochemistry 49(10): 1177-1182.
74. Cappellari LR, Chiappero J, Palermo TB, Giordano W, Banchio E (2020) Volatile organic compounds from rhizobacteria increase the biosynthesis of secondary metabolites and improve the antioxidant status in Mentha piperita grown under salt stress. Agronomy 10(8): 1094.
75. Bambal AS, Verma RM, Panchbhai DM, Mahorkar VK, Khankhane RN (1998) Effect of biofertilizers and nitrogen levels on growth and yield of cauliflower (Brassica oleracea var. botrytis). Orissa J Hort 26(2): 14-17.
76. Panwar JDS, Singh O (2000) Response of Azospirillum and Bacillus on growth and yield of wheat under field conditions. Indian J Plant Physiol 5: 108-110.
77. Omar MNA, Fang P, Jia XM (2000) Effect of inoculation with Azospirillum brasilense NO40 isolated from Egyptian soils on rice growth in China. Egypt J Agric Res 78(3): 1005-1014.
78. Bashan Y, Bustillos JJ, Leyva LA, Hernandez JP, Bacilio M (2006) Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biol Fertil Soils 42: 279-285.
79. Glick BR, Bashan Y (1997) Genetic manipulation of plant growth-promoting bacteria to enhance biocontrol of phytopathogens. Biotechnology Advances 15(2): 353-378.
80. Al-Whaibi MH (2008) Plant growth promoting rhizobacteria. Saudi Journal of Biological Sciences 15(3): 3-16.
81. Madigan MT, Martinko JM, Parker J (2000) Brock biology of microorganisms. (8^th edn), Prentice-Hall Inc, Englewood Cliffs, New Jersey, USA.
82. Thomashow LS, Weller DM (1998) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. Journal of Bacteriology 170(8): 3499-3508.
83. Sottero AN, Freitas S, Melo AMT, Trani PE (2006) Rhizobacteria and lettuce: Root colonization, plant growth, promotion and biological control. Rev Bras Ciênc Solo 30(2): 225-234.
84. Sharma A, Wray V, Johri BN (2007) Rhizosphere Pseudomonas sp strains reduce occurrence of pre- and post-emergence damping-off in Chile and tomato in central Himalayan region. Archives of Microbiology 187(4): 321-335.
85. Weisbeek PJ, Gerrits H (1999) Iron and biocontrol. In: Stacey G, Keen NT (Eds.), Plant-Microbe Interactions, APS Press, St. Paul, Minnesota, USA, pp. 217-250.
86. Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, Van Loon LC (2002) Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol 4: 535-544.
87. Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36: 453-483.
88. Chanway CP (1997) Inoculation of tree roots with plant growth promoting soil bacteria: An emerging technology for reforestation. For Sci 43(1): 99-112.
89. Kloepper JW(1993) Plant growth-promoting rhizobacteria as biological control agents. In: Metting B (Ed.), Soil Microbial Ecology: Applications in Agricultural and Environmental Management, Marcel Dekker, New York, USA, pp. 255-274.
90. Ramos B, García JAL, Probanza A, Barrientos ML, Gutiérrez Mañero FJ (2003) Alterations in the rhizobacterial community associated with European alder growth when inoculated with PGPR strain Bacillus licheniformis. Environmental and Experimental Botany 49(1): 61-68.
91. Domenech J, Ramos-Solano B, Probanza A, Lucas-Garcia JA, Colon JJ, et al. (2004) Bacillus and Pisolithus tinctorius effects on Quercus ilex ssp. ballota a study on tree growth, rhizosphere community structure and mycorrhizal infection. Forest Ecology and Management 194(1-3): 293-303.
92. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany 52(Suppl 1): 487-511.
93. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 3(4): 307-319.
94. Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines and their role in biocontrol by Pseudomonas New Phytologist 157(3): 503-523.
95. Kishore GK, Pande S, Podile AR (2005) Management of late leaf spot of groundnut (Arachis hypogaea) with chlorothalonil-tolerant isolates of Pseudomonas aeruginosa. Plant Pathology 54(3): 401-408.
96. Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 21(5): 573.
97. Andreote FD, Pereira ESMC (2001) Microbial communities associated with plants: Learning from nature to apply it in agriculture. Curr Opin Microbiol 37: 29-34.
98. Backer RGM, Saeed W, Seguin P, Smith DL (2017) Root traits and nitrogen fertilizer recovery efficiency of corn grown in biochar-amended soil under greenhouse conditions. Plant Soil 415: 465-477.
99. Akladious SA, Abbas SM (2012) Application of Trichoderma harziunum T22 as a biofertilizer supporting maize growth. Afr J Biotechnol 11(35): 8672-8683.
100. Molla AH, Haque MM, Haque MA, Ilias G (2012) Trichoderma-enriched biofertilizer enhances production and nutritional quality of tomato (Lycopersicon esculentum mill.) and minimizes NPK fertilizer use. Agric Res 1: 265-272.
101. Niu DD, Zheng Y, Zheng L, Jiang CH, Zhou DM, et al. (2016) Application of PSX biocontrol preparation confers root-knot nematode management and increased fruit quality in tomato under field conditions. Biocontrol Sci. Technol 26(2): 174-180.
102. Shakeri E, Modarres-Sanavy SAM, Amini Dehaghi M, Tabatabaei SA, Moradi-Ghahderijani M (2016) Improvement of yield, yield components and oil quality in sesame (Sesamum indicum) by N-fixing bacteria fertilizers and urea. Arch Agron Soil Sci 62(4): 547-560.
103. Nosheen A, Bano A, Ullah F (2016) Bioinoculants: A sustainable approach to maximize the yield of Ethiopian mustard (Brassica carinata) under low input of chemical fertilizers. Toxicol Ind Health 32(2): 270-277.
104. Nosheen A, Bano A, Yasmin H, Keyani R, Habib R, et al. (2016) Protein quantity and quality of safflower seed improved by NP fertilizer and Rhizobacteria (Azospirillum and Azotobacter). Front Plant Sci 7: 104.
105. Ajjawi I, Verruto J, Aqui M, Soriaga LB, Coppersmith J, et al. (2017) Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nat Biotechnol 35(7): 647-652.
106. Rokem JS, Greenblatt CL (2015) Making biofuels competitive: The limitations of biology for fuel production. JSM Microbiol 3(2): 1023.
107. Evangelou MW, Deram A (2014) Phytomanagement: A realistic approach to soil remediating phytotechnologies with new challenges for plant science. Int J Plant Biol Res 2: 1023.
108. Kuhad RC, Gupta R, Singh A (2011)Microbial cellulases and their industrial applications. Enzyme Res 2011: 280696.
109. Margaritopoulou T, Roka L, Alexopoulou E, Christou M, Rigas S, et al. (2016) Biotechnology towards energy crops. Mol Biotechnol 58(3): 149-158.
110. McCalmont JP, Hastings A, Mcnamara NP, Richter GM, Robson P, et al. (2017) Environmental costs and benefits of growing Miscanthus for bioenergy in the UK. Glob Chang Biol Bioenergy 9(3): 489-507.
111. Ker K, Seguin P, Driscoll BT, Fyles JW, Smith DL (2012) Switchgrass establishment and seeding year production can be improved by inoculation with rhizosphere endophytes. Biomass Bioenergy 47: 295-301.
112. Ker K, Seguin P, Driscoll BT, Fyles JW, Smith DL (2014) Evidence for enhanced N availability during switchgrass establishment and seeding year production following inoculation with rhizosphere endophytes. Arch Agron Soil Sci 60(11): 1553-1563.
113. Shanta N, Schwinghamer T, Backer R, Allaire SE, Teshler I, Vanasse A, et al. (2016) Biochar and plant growth promoting rhizobacteria effects on switchgrass (Panicum virgatum Cave-in-rock) for biomass production in southern Québec depend on soil type and location. Biomass Bioenergy 95: 167-173.
114. Arunachalam S, Schwinghamer T, Dutilleul P, Smith DL (2017) Multi-year effects of biochar, lipo-chitooligosaccharide, thuricin 17, and experimental bio-fertilizer for switchgrass. Agron J 110(1): 77-84.
115. Harman GE (2000) Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzinum T-22. Plant Dis 84: 377-393.
116. Velivelli SL, De Vos P, Kromann P, Declerck S, Prestwich BD (2014) Biological control agents: From field to market, problems, and challenges. Trends Biotechnol 32(10): 493-496.
117. Doumbou CL, Salove MKH, Crawford DL, Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82(3): 85-102.
118. Company S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71(9): 4951-4959.
119. Prashar P, Kapoor N, Sachdeva S (2013) Biocontrol of plant pathogens using plant growth promoting bacteria. In: Lichtfouse E (Ed.), Sustainable Agriculture Reviews, Springer, Dordrecht, Netherlands, pp. 319-360.